Abstract
ABSTRACTMembers of the bacterial phylum Gemmatimonadota are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil. Sequences affiliated with Gemmatimonadota were also reported from diverse aquatic habitats; however, it remains unknown whether they are native organisms or represent bacteria passively transported from sediment or soil. To address this question, we analyzed metagenomes constructed from five freshwater lakes in central Europe. Based on the 16S rRNA gene frequency, Gemmatimonadota represented from 0.02 to 0.6% of all bacteria in the epilimnion and between 0.1 and 1% in the hypolimnion. These proportions were independently confirmed using catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH). Some cells in the epilimnion were attached to diatoms (Fragilaria sp.) or cyanobacteria (Microcystis sp.), which suggests a close association with phytoplankton. In addition, we reconstructed 45 metagenome-assembled genomes (MAGs) related to Gemmatimonadota. They represent several novel lineages, which persist in the studied lakes during the seasons. Three lineages contained photosynthesis gene clusters. One of these lineages was related to Gemmatimonas phototrophica and represented the majority of Gemmatimonadota retrieved from the lakes’ epilimnion. The other two lineages came from hypolimnion and probably represented novel photoheterotrophic genera. None of these phototrophic MAGs contained genes for carbon fixation. Since most of the identified MAGs were present during the whole year and cells associated with phytoplankton were observed, we conclude that they represent truly limnic Gemmatimonadota distinct from the previously described species isolated from soils or sediments.IMPORTANCE Photoheterotrophic bacterial phyla such as Gemmatimonadota are key components of many natural environments. Its first photoheterotrophic cultured member, Gemmatimonas phototrophica, was isolated in 2014 from a shallow lake in the Gobi Desert. It contains a unique type of photosynthetic complex encoded by a set of genes which were likely received via horizontal transfer from Proteobacteria. We were intrigued to discover how widespread this group is in the natural environment. In the presented study, we analyzed 45 metagenome-assembled genomes (MAGs) that were obtained from five freshwater lakes in Switzerland and Czechia. Interestingly, it was found that phototrophic Gemmatimonadota are relatively common in euphotic zones of the studied lakes, whereas heterotrophic Gemmatimonadota prevail in deeper waters. Moreover, our analysis of the MAGs documented that these freshwater species contain almost the same set of photosynthesis genes identified before in Gemmatimonas phototrophica originating from the Gobi Desert.
Highlights
Members of the bacterial phylum Gemmatimonadota are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil
With the discovery of Gemmatimonas phototrophica, which contains photosynthetic reaction centers [14, 15], Gemmatimonadota were added to several bacterial phyla containing anoxygenic phototrophic species alongside Proteobacteria, Chlorobi, Chloroflexota, Firmicutes (Bacillota), Acidobacteriota, and the newly discovered phylum “Candidatus Eremiobacterota” (WPS-2) [14, 16, 17]
The gene arrangement in the photosynthesis gene cluster (PGC) of G. phototrophica is very similar to the one found in Proteobacteria, so it has been suggested that phototrophy in Gemmatimonadota originates from an ancient horizontal gene transfer of the entire PGC from Proteobacteria [14]
Summary
Members of the bacterial phylum Gemmatimonadota are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil. With the discovery of Gemmatimonas phototrophica, which contains photosynthetic reaction centers [14, 15], Gemmatimonadota were added to several bacterial phyla containing anoxygenic phototrophic species alongside Proteobacteria, Chlorobi ( included as a class-level lineage in Bacteroidota [2]), Chloroflexota, Firmicutes (Bacillota), Acidobacteriota, and the newly discovered phylum “Candidatus Eremiobacterota” (WPS-2) [14, 16, 17]. Anoxygenic phototrophs, such as G. phototrophica, are able to support their metabolism by harvesting light using bacteriochlorophylls; they require a supply of organic substrate for growth [18]. This is the only known case of horizontal transfer of an entire set of photosynthesis genes between distant bacterial phyla [14, 19]
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